Journal of Science (2017) 17(2): 37; 1–8 doi: 10.1093/jisesa/iex001 Research article

Modeling Temperature-Dependent Development of pyloalis (: Pyralidae)

Zohreh Moallem, Azadeh Karimi-Malati,1 Ahad Sahragard, and Arash Zibaee

Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht, and 1Corresponding author, e-mail: [email protected] Subject Editor: Sunil Kumar

Received 3 October 2016; Accepted 27 December 2017

Abstract Development of Walker was studied under laboratory conditions at constant temperatures of 12, 16, 20, 24, 28, 30, 32, and 36 C. No development occurred at 36 C. Although eggs hatched at 12 C, no lar- vae were capable of developing to adult stage. At 16 C, survival rate was low (4%) and prepupal stage lasted 101.68 6 11.03 d. Larvae completed development through six stadia at 16, 30, and 32 C. Developmental time of overall immature stages varied from 46.62 d at 20 C to 22.04 d at 30 C and increased at 32 C. The lower tem- perature thresholds of 10.30 and 11.22 C, and thermal constants of 429.18 and 401.88 DD were estimated by

traditional and Ikemoto–Takai linear models, respectively. The Tmin values estimated by Analytis, Briere-2, Lactin-2, and Sharpe–Schoolfield–Ikemoto (SSI) for overall immature stages were 12.40, 12.92, 9.00, and 13.04 C, respectively. The fastest development temperatures (Tfast) of 31.1, 31.1, 30.8, and 30.7 C were esti- mated for overall immature stages based on Analytis, Briere-2, Lactin-2, and SSI, respectively. The intrinsic opti-

mum temperature (Topt) estimated from the thermodynamic SSI model for total developmental time was 24.63 C, in which the maximal active state enzymes involved in developmental process. The nonlinear models

of Analytis, Lactin-2, Briere-2, and SSI estimated the upper temperature thresholds (Tmax) at 36.66, 35.97, 38.88, and 34.05 C, respectively. These findings could be used to predict the population dynamics of G. pyloalis for an effective management.

Key words: degree day, Glyphodes pyloalis, temperature threshold, thermal model

The lesser mulberry pyralid, Glyphodes pyloalis Walker nutritional indices of G. pyloalis larvae (Oftadeh et al. 2014), as well (Lepidoptera: Pyralidae), is a specialist pest on mulberry ( as its life table parameters (Oftadeh et al. 2015) were determined under spp.) and is widely distributed throughout Asia, where the species laboratory conditions. Furthermore, the influence of abiotic climate causes serious damage to sericulture not only by its larval grazing on factors on incidence and severity (Ramegowda et al. 2012) and damage leaves but also by transmission of some viral diseases infectious to rate of G. pyloalis (Borgohain et al. 2015) was described to evolve a the silkworm (Watanabe et al. 1988, Madyarov et al. 2006). On the successful IPM program. According to Borgohain et al. (2015),the other hand, G. pyloalis becomes a major pest of mulberry as shade evening relative humidity and minimum temperature had significant trees in urban area (Kumar et al. 2002). Recently, this pest has positive effects on occurrence of G. pyloalis. caused severe damage to mulberry plantations in northern Iran espe- It should be considered that among the climatic factors, tempera- cially Guilan province. The leaf area eaten by the first and second in- ture is the most important, as it has profound influence on the devel- star larvae is negligible, but feeding increases in later instars, and opment and survival of . The insect developmental rate, as fifth instar larvae feed whole leaf and finally only the ribs remain poikilothermic organism, is affected by the temperature to which in- (Khosravi and Jalali Sendi 2010). Since the larvae of the pest defoli- sects are exposed (Davidson 1944, Campbell et al. 1974). In fact, ate mulberry and finally lead to plant death, some investigations temperature is a critical factor that influences pest biology, distribu- were done to know its biological parameters and control tools. tion and abundance, as well as its population dynamics (Braman Khosravi and Jalali Sendi (2010) studied the demographic param- et al. 1984, Tobin et al. 2003, Zahiri et al. 2010). Attempts to quan- eters of G. pyloalis and its behavioral aspects. Yazdani et al. (2014) tify the effects of temperature on developmental rate, growth, fe- stated that the essential oils of Thymus vulgaris L. and Origanum cundity and enzyme activities have been carried out by several vulgare L. were effective for G. pyloalis control through disturbance studies for different insect and mite species (Kontodimas et al. 2004, on activity of macromolecules, digestive and detoxifying enzymes. Zahiri et al. 2010, Jafari et al. 2012, Karimi-Malati et al. 2014). In Moreover, the effects of different mulberry varieties on the addition, a variety of temperature-driven rate models have been

VC The Authors 2017. Published by Oxford University Press on behalf of Entomological Society of America. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unre- stricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 2 Journal of Insect Science, 2017, Vol. 17, No. 2 proposed to describe the relationship between temperature and in- cocooned pupae were checked and the emerged adults recorded sect development (Sharpe and DeMichele 1977; Analytis 1981; daily. Developmental time of different and overall immature stages Schoolfield et al. 1981; Lactin et al. 1995; Briere et al. 1999; Shi was recorded based on regular observations with 24 h intervals. et al. 2011a,b). Several studies revealed that there is no development at temperatures below the lower threshold. While as temperature Thermal Models rises, developmental rates increase up to an optimum temperature, The reciprocal of developmental time for different stages of G. pyloalis above which they again decrease and eventually cease at their upper was calculated to obtain the developmental rate. Two linear, tradi- threshold (Sharpe and DeMichele 1977, Analytis 1981, Briere et al. tional and Ikemoto–Takai models were applied to estimate the 1999). Based on linear models, lower temperature threshold and temperature-dependent development of egg, larval, prepupal, pupal, thermal constant can be estimated at moderate temperatures. and total immature stages of G. pyloalis on mulberry leaves. The tradi- However, linear models proved unsecure in predicting developmen- tional and Ikemoto–Takai models are as follows, respectively: tal rate near extreme conditions, therefore, nonlinear models have 1 T T been proposed to describe developmental rate response curves over ¼ min þ (1) D K K the broad range of temperatures (Wagner et al. 1984).

Although different climate factors affecting occurrence and in- DT ¼ K þ TminD (2) festation of G. pyloalis were considered (Ramegowda et al. 2012, where D is the duration of development (days), T is the ambient Borgohain et al. 2015), no information exists on the relationship of temperature, T is the lower temperature threshold, and K is the its developmental rate and temperature. This study was conducted min thermal constant (degree day, DD). to assess the developmental rate of G. pyloalis at eight constant tem- The latter function is a new linearized formula was proposed by peratures and estimate the temperature thresholds and thermal re- Ikemoto and Takai (2000). Ikemoto and Takai (2000) particularized quirements, which would be useful in developing models for some problems regarding the traditional linear model would result in a predicting its distribution and abundance. Predicting the seasonal lower T and larger K, hence, equation (2) is derived from the tradi- occurrence of G. pyloalis based on climate factors such as tempera- min tional linear model to obtain more reliable estimates of the parameters. ture is essential for its accurate scheduling of census samples and It should be considered that the relationship between tempera- control tactics. Two linear and four nonlinear models were used for tures and developmental rate is curvilinear near lower and upper estimating accurate thermal constant and temperature thresholds of temperature thresholds. To describe the developmental rate over a G. pyloalis, which would be useful in developing phenological mod- wider temperature range, four nonlinear models including Analytis, els and constructing an effective pest management program. Briere-2, Lactin-2, and Sharpe–Schoolfield–Ikemoto (SSI) were chosen (Analytis 1981, Lactin et al. 1995, Briere et al. 1999, Shi Materials and Methods et al. 2011b). These four mentioned nonlinear formulations are as follows, respectively: Rearing Methods

The larvae of G. pyloalis were collected from mulberry trees in 1 n m ¼ a ðT TminÞ ðTmax TÞ (3) Rasht, Guilan province, Iran during 2015. They were reared at labo- D ratory conditions at 25 6 1 C and 70 6 10% RH, with a photoper- 1 ¼ a TTðÞð T T TÞ1=d (4) iod of 16:8 L:D h on fresh mulberry leaves. To obtain the same aged D min max eggs, female and male (15 pairs) were kept inside the oviposi- tion containers (50 50 50 cm) with a 10% honey solution on 1 Tmax T ¼ expðÞp T exp p Tmax þ k (5) cotton wool for feeding and mulberry leaves for oviposition. D DT

where Tmin is the lower temperature threshold, Tmax is the upper Development and Survivorship of Immature Stages temperature threshold, a, d, n, m, p, k, and DT are fitted coefficients After mating and oviposition, one hundred to 300 (depending thermal (Analytis 1981, Briere et al. 1999, Roy et al. 2002, Kontodimas treatment) freshly laid eggs (< 24 h old) were transferred to plastic et al. 2004). In addition, the SSI model was used in this research boxes (18 15 7 cm) with wet cotton wool in growth chambers at which is closely related to the impact of temperature on the enzyme. eight constant temperatures of 12, 16, 20, 24, 28, 30, 32, and Using SSI model enable researchers to estimate the intrinsic opti- 36 6 1 Cat706 10% R.H. and photoperiod of 16:8 L:D h. mum temperature (Topt) in which the population size is maximal Changing in shape and color of eggs was monitored daily under the with a low mortality (Ikemoto 2005, 2008, Shi et al. 2011b). stereomicroscope. Incubation period and hatching rate were recorded. Ikemoto (2005) and Shi et al. (2011b) demonstrated that the intrin- The newly hatched larvae were placed individually in plastic sic optimum temperature (Topt) should represent a temperature at containers (7 8 3 cm) with a hole in their lids covered by a fine which the mortality of insects is very low, and that the net reproduc- mesh to provide ventilation. The petioles of mulberry leaves were tive rate is generally highest. In fact, Topt is different from Tfast that kept in tubes containing water to keep the cutting leaves as fresh as make insects develop fastest within shortest duration: possible. The leaves were replaced every other day for larvae at 1 q ðT=T Þexp½DH =R ðð1=T Þð1=TÞÞ 16–24 C and daily for those larvae at 28–32 C because plant desic- ¼ U opt A opt D 1 þ exp½DHL =R ðð1=TLÞð1=TÞÞ þ exp½DHH=R ðð1=THÞð1=TÞÞ cation occurred faster than lower temperatures. The larvae were [6] checked and the instars were regularly recorded using the exuviae of larval head capsules. The matured larvae changed color from green where qU is the mean developmental rate at Topt (1/d), Topt is the to purple and began making fine cocoons considering prepupal intrinsic optimum temperature at which the probability of an stage. After pupation, they were slipcovered and sexes were deter- enzyme being in the active state is maximal. DHA, DHL, and DHH mined based on morphological characters of pupal last abdominal are the enthalpy of activation of the reaction that is catalyzed by the segment. After that they were replaced in their fine cocoons. The enzyme (cal/mol), the change in enthalpy associated with low Journal of Insect Science, 2017, Vol. 17, No. 2 3 temperature inactivation of the enzyme (cal/mol), and the change in Thermal constant (K), the amount of thermal energy (DD) enthalpy associated with high temperature inactivation of the needed to complete development of different stages. The thermal enzyme (cal/mol), respectively, R is the gas constant (1.987 cal/deg/ constant can be estimated only by the linear equation. The SE of K mol), TL is the temperature at which the enzyme is 1/2 active and was estimated by using the following equation (Campbell et al.

1/2 low temperature inactive, and TH is the temperature at which 1974, Kontodimas et al. 2004). the enzyme is 1/2 active and 1/2 high temperature inactive (Both in SE SE ¼ b [8] Kelvin degrees). K b2 Since running the SSI model through Ikemoto (2008) takes 3 h for an average personal computer, a modified mentioned program was proposed by Shi et al. (2011b) to speed up the estimation of Statistical Analysis model parameters. Normality of distribution was checked with the Kolmogorov– Smirnov test before comparative analyses were performed. Effect of Critical Temperatures and Parameter Estimation temperature on developmental periods of G. pyloalis was analyzed Critical temperatures and thermal requirement of G. pyloalis were by one-way analysis of variance ANOVA (PROC GLM, SAS estimated by above-mentioned models. Institute 2007) and means were separated using Tukey Honestly Significant Difference HSD multiple comparison (P 0.01). The lin- The lower temperature threshold (Tmin), the temperature below ear models were analyzed using statistical software MINITAB 16.0 which different stages did not develop. The standard error (SE) of and nonlinear models analyzed using linear and nonlinear platforms Tmin calculated from the linear models is of JMP, v 7.0 (SAS Institute 2007). For estimating the parameters of sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi r S2 SE 2 the SSI model, a program which runs on R software was used at the SE ¼ þ b [7] Tmin b N r2 b present study (Shi et al. 2011b). where S2 is the residual mean square of r, r is the sample mean, and N isthesamplesize(Campbell et al. 1974, Kontodimas et al. Results 2004). Developmental Time and Mortality The upper temperature threshold (Tmax), the temperature above The mean developmental time of each immature stage of G. pyloalis which the life cannot be maintained for any significant period at six constant temperatures are shown in Table 1. The results of (Kontodimas et al. 2004). This value was estimated only by the non- developmental time and survival rate showed that G. pyloalis was linear models. able to complete its life cycle and development at a wide range tem-

The fastest development temperature (Tfast), defined as the tem- perature. In fact, the adults were capable of emergence across a perature at which the highest developmental rate was recorded. range of 20–32 C, whereas few eggs developed to adult stage at However, the fitness of population is usually not maximal because 16 C (with 4% survivorship; only six emerged adults). As far as pre- of the higher mortality at Tfast. pupal stage is concerned, at 16 C G. pyloalis required

Table 1. Developmental time (means 6 SE) and survival of Glyphodes pyloalis immature stages at constant temperatures

Temperature (C)

Stage 16 20 24 28 30 32

Egg 9.75 6 0.07a 6.52 6 0.04b 4.76 6 0.04c 3.71 6 0.05d 3.00 6 0.00e 3.00 6 0.00e no (s) 150 (65.71) 112 (70.38) 107 (83.53) 80 (87.50) 106 (77.36) 84 (61.90) Larva I 8.92 6 0.18a 4.97 6 0.09b 3.15 6 0.07c 2.38 6 0.10d 2.00 6 0.00e 2.45 6 0.10d no (s) 97 (91.75) 78 (85.90) 89 (100) 59 (100) 82 (100) 52 (100) Larva II 6.48 6 0.14a 3.68 6 0.10b 2.41 6 0.06c 2.00 6 0.04d 1.04 6 0.03e 1.84 6 0.10d no (s) 89 (94.38) 67 (98.51) 89 (97.75) 59 (94.92) 82 (100) 52 (100) Larva III 6.18 6 0.13a 4.00 6 0.12b 2.15 6 0.05c 2.06 6 0.03cd 1.76 6 0.06d 1.95 6 0.10cd no (s) 84 (90.48) 66 (93.94) 87 (97.70) 56 (100) 82 (95.12) 52 (98.08) Larva IV 6.72 6 0.17a 5.53 6 0.15b 2.64 6 0.07c 2.44 6 0.07cd 1.88 6 0.05e 2.00 6 0.08de no (s) 76 (85.53) 62 (96.77) 85 (98.82) 56 (94.64) 78 (94.87) 51 (100) Larva V 8.22 6 0.16a 6.18 6 0.13b 3.72 6 0.08c 2.87 6 0.09d 3. 07 6 0.07d 2.74 6 0.16d no (s) 65 (83.08) 60 (100) 84 (96.43) 53 (98.11) 74 (93.24) 51 (86.27) Larva VIa 8.33 6 1.33a – – – 4.50 6 1.15b 2.67 6 0.19b no (s) 54 (92.59) – – – 69 (98.55) 44 (86.36) Larvae 37.02 6 0.34a 24.37 6 0.31b 14.06 6 0.12c 11.75 6 0.13d 10.16 60.18e 11.89 6 0.28d no (s) 97 (51.55) 78 (76.92) 89 (91.01) 59 (88.14) 82 (82.93) 52 (73.08) Pre pupab 101.68 6 11.03 4.64 6 0.11a 2.28 6 0.05b 1.94 6 0.03c 2.11 6 0.06bc 2.25 6 0.19bc no (s) 50 (38) 60 (83.33) 81 (96.30) 52 (100) 68 (92.65) 38 (84.21) Pupab 24.67 6 1.61 12.32 6 0.14a 8.62 6 0.07b 7.08 6 0.05c 6.80 6 0.09c 6.14 6 0.08d no (s) 19 (31.57) 50 (94) 78 (87.18) 52 (98.08) 63 (85.71) 32 (65.63) Immatureb 134.33 6 25.19 46.62 6 0.23a 29.34 6 0.17b 24.47 6 0.17c 22.04 6 0.20d 22.43 6 0.25d

No, sample size; s, survival (%). Means within rows followed by the same letters are not significantly different (P < 0.05). aAt 20, 24, and 28 C larvae completed development in five stadia. bComparing the prepupal, pupal, and total developmental times was done without considering of the temperature at 16 C. 4 Journal of Insect Science, 2017, Vol. 17, No. 2

101.68 6 11.03 d to develop to pupal stage maybe due to stop devel- occurred at 12 C, all neonate larvae died due to the exposure to low oping (or diapause occurrence) in prepupal stage. For these two rea- temperature. Furthermore, survival of total larval stage of G. pyloa- sons, too long duration and low survivorship of prepupal stage both lis at six constant temperatures revealed that the survival was high- occurred at 16 C, developmental times of prepupal, pupal, and total est (65%) at 28 C, followed by 24 C(Table 1). immature stages were ignored and comparing the mean duration of above-mentioned stages (prepupal, pupal, and total developmental Model Evaluations times) was done without considering of the temperature at 16 C The developmental rate of G. pyloalis increased linearly within the (Table 1). examined temperature range (20–30 C). Developmental time According to our results, eggs could hatch after 17.72 6 0.86 d at >30 C (32 C) was outside the linear segment of the growth at 12 C without any surviving to the next stage and all neonate lar- curve and therefore excluded from the linear regression. Results of vae died. In addition, at 36 C, no eggs hatched. Developmental parameter estimation of linear models (traditional and Ikemoto– 2 2 time for each stage was significantly influenced by temperature: Takai), coefficients of determination (R and R adj), lower tempera- incubation period (F ¼ 2961.97; df ¼ 5, 742; P < 0.0001), ture thresholds and thermal constants are presented in Table 2. The larval (F ¼ 1941.75; df ¼ 5, 348; P < 0.0001), prepupal (F ¼ 173.14; estimated lower temperature thresholds for total developmental df ¼ 4, 274; P < 0.0001), pupal (F ¼ 670.42; df ¼ 4, 240; time were 10.30 and 11.22 C, while the thermal constants were P < 0.0001), and overall immature stages (F ¼ 2479.46; df ¼ 4, 240; 429.18 and 401.88 DD, using the traditional and Ikemoto–Takai P < 0.0001) (Table 1). The larval developmental time ranged linear models, respectively. The thermal requirements were lowest 24.37 6 0.31 to 10.16 6 0.18 d at 20 and 30 C, respectively. at the prepupal stage and the highest at the larval stage. The curves Moreover, comparing the number of stadia in larval stage indicated of influence of temperature on developmental rate of overall imma- that an extra (sixth) stadium was observed at extreme temperatures ture stages fitted by two linear models are shown in Fig. 1. (16, 30, and 32 C). In fact, no larvae required more than five stadia Four nonlinear models (Analytis, Briere-2, Lactin-2, and SSI) at 20, 24, and 28 C. were fitted to the data on developmental rate of egg, larval, prepu- The survival rate of overall immature stages indicated that the pal, pupal, and overall immature stages of G. pyloalis at the temper- 2 lowest survival rate occurred at 16 C (4%). Although egg hatching ature range from 20 to 32 C(Table 3). The values of R adj were

Table 2. Lower temperature threshold (Tmin 6 SE) and thermal constant (K 6 SE) of immature stages of Glyphodes pyloalis estimated by lin- ear models

2 2 Stage Regression equation R % R adj% PTmin K

Traditional linear Egg 1/D ¼0.197 þ 0.0172 T 97.10 95.70 0.014 11.45 6 1.77 58.14 6 7.07 Larvae 1/D ¼0.0658 þ 0.00548 T 97.60 96.40 0.01 12.01 6 1.54 182.48 6 20.16 Prepupa 1/D ¼0.508 þ 0.0374 T 92.65 85.30 0.11 13.58 6 5.87 26.74 6 13.87 Pupa 1/D ¼0.0786 þ 0.00801 T 99.14 98.70 0.004 9.81 6 2.02 124.84 6 16.27 Immature 1/D ¼0.0240 þ 0.00233 T 98.06 97.09 0.009 10.30 6 1.58 429.18 6 43.09 Ikemoto–Takai linear Egg DT ¼ 60.278 þ 10.977 D 97.23 95.85 0.013 10.98 6 1.3 60.28 6 6.14 Larvae DT ¼ 170.22 þ 12.89 D 98.68 98.02 0.006 12.89 6 1.05 170.22 6 16.92 Prepupa DT ¼ 23.19 þ 14.9 D 98.86 97.71 0.06 14.93 6 1.60 23.19 6 5.12 Pupa DT ¼ 124.14 þ 9.89 D 98.81 98.21 0.006 9.89 6 0.76 124.14 6 6.79 Immature DT ¼ 401.88 þ 11.22 D 97.93 96.89 0.01 11.22 6 1.15 401.88 6 37.04

Developmental times at 16 and 34 C were excluded from linear regressions.

Traditional linear model Ikemoto-Takai model 0.06 1200 ) -1 0.05 1000

0.04 800

0.03 600

0.02 400

0.01 200 Developmental rate (day rate Developmental Development ×Development Temperature 0 0 0 5 10 15 20 25 30 35 40 45 0 5 10 15 20 25 30 35 40 45 50 Temperature (ºC) Development (day)

Fig. 1. Fitting the linear models (line) to observed developmental rates (•) of Glyphodes pyloalis. Journal of Insect Science, 2017, Vol. 17, No. 2 5 used to determine the goodness of fit the models. The adjusted coef- 24 6 1 C. Similarly working with G. pyloalis on four mulberry vari- 2 ficients of determination (R adj) in all tested models for overall eties, Oftadeh et al. (2015) stated that the egg incubation periods immature stages were higher than 0.95. The curves of the relation- varied from 3.77 to 4.44 d at 24 6 1 C. Our results for incubation ship between temperature and developmental rate of total immature period of G. pyloalis at same temperature agreed with those stages fitted by mentioned models are depicted in Fig. 2. reported by Khosravi and Jalali Sendi (2010) and Oftadeh et al. The results of present study showed that the lower developmen- (2015). Moreover, Khosravi and Jalali Sendi (2010), and Oftadeh tal thresholds (Tmin) for overall immature stages estimated by the et al. (2015) reported that the larval stage of G. pyloalis required Analytis, Briere-2, and Lactin-2 were 12.4, 12.92, and 9 C, respec- five stadia, however, an extra (sixth) stadium was observed at 16, tively. Moreover, the SSI model estimated TL for overall immatures 30, and 32 C at present study. These differences may be due to stage at 13.04 C, in which the hypothetical enzyme was half active larval body size depending on very high- or low-developmental rate and half inactive. Based on current study, the Analytis, Briere-2, at extreme temperatures. Shi et al. (2013) emphasized that both pop-

Lactin-2, and SSI models estimated Tfast for overall immature stages ulation size and body size are important in fitness of ectotherms, at 31.1, 31.1, 30.8, and 30.7 C, respectively. In estimated Tfast indicating developmental times are based on the particular morphol- developmental time is shortest but the fitness of population is usu- ogy and size of the species at different temperatures (Honek 1996). ally not maximal because of the higher mortality. Whereas the esti- Therefore, an extra molting might be justifiable for larval stage of mates of Topt using SSI model for different stages varied from 22.66 G. pyloalis at extreme temperatures. to 28.21 C which represented the optimal temperature for According to the present study, it should be considered that pre- G. pyloalis population to develop with a low mortality. pupal developmental times were 4.64, 2.28, 1.94, 2.11, and 2.25 d at 20, 24, 28, 30, and 32 C, respectively, whereas at 16 C prepupal developmental time prolonged 101.68 d. It seems that this longest Discussion prepupal developmental time observed at 16 C may be related to The estimated temperature thresholds and thermal constants are less tolerance to low temperatures which could stop development potential indicators for developing a phenology model of G. pyloalis and prolong this stage. Few researchers have focused on overwinter- and predicting its population dynamics. According to the surveys, so ing or diapause of G. pyloalis under field conditions. Mathur (1980) far research study has not been done regarding to critical tempera- monitored life history of G. pyloalis during 1933–1934 and stated tures (Tmin, Tmax, Topt) and thermal requirements of the lesser mul- that the matured larvae of last generation made the cocoons and berry pyralid. The biology of the pest was examined by Khosravi hibernated inside the leaves on the ground from mid-autumn. Based and Jalali Sendi (2010) under laboratory conditions, who demon- on Mathur (1980), no hibernation of pupae occurred and overwin- strated that the incubation period of G. pyloalis was 4.06 d at tering larvae pupated in next early March. The findings of present

Table 3. Estimated parameters and goodness of fit of the nonlinear models fitting to developmental rates of Glyphodes pyloalis

Model Parameters Egg Larva Prepupa Pupa Immature

Analytis a 0.0180805941 0.0093445459 0.0026737994 0.0099970236 0.00006334287

Tmin 12.087979091 14.55 15.977576718 10.953642573 12.4

Tmax 32 32.002136251 37.028156352 32 36.659062923 n 0.9971826195 0.8459044687 1.2959553193 0.944708698 1.2456828095 m 0.0020776935 0.0360820395 0.9232286618 0.0026302548 0.3586178111

Tfast 31.9 31.9 28.3 31.9 31.1 2 R adj 0.9711 0.9782 0.9465 0.9907 0.9898 Briere-2 a 0.0006457008 0.0000707783 0.0002463701 0.0002935356 0.000035978 d 4432866.14 1.7128474553 1.1378065837 38099.29866 1.9929415702

Tmin 12.85 14.159022666 16.037315313 9.575530105 12.923886455

Tmax 32.111 35.649026102 36.031026187 30.77 35.968777953 Tfast 32.9 30.4 27.7 31.9 31.1 2 R adj 0.9529 0.9548 0.9655 0.9829 0.9817 Lactin-2 p 0.0125922236 0.0049437231 0.1096400671 0.0067671533 0.1238102145 DT 0.0813549794 0.7008941528 8.687924051 0.0778880862 8.0661967712 k 1.138739779 1.060232293 0.590717205 1.063005565 0.014783871

Tmax 32.336013185 34.649397346 37.653561342 32.339177483 38.88 Tmin 10.3 11.9 14.8 9.1 9.0

Tfast 31.8 30.6 28.6 31.3 30.8 2 R adj 0.9764 0.9682 0.9326 0.9912 0.9853 SSI qU 0.2866211 0.06756835 0.3332183 0.1108385 0.03337244

Topt 28.2088 24.3899 22.663 23.654 24.6338 TL 11.13197 12.97607 16.9636 9.950553 13.0422

TH 32.451 32.8627 31.4021 35.0202 34.0533 DHA 13,292.41 15,236.67 20,317.41 12,144.71 13,205.04

DHL 76,643.64 138,159.7 127,233.6 143,849.7 73,234.83 DHH 786,228.6 122,641.5 76,757.69 92,395.43 103,394 Tfast 31.5 30 29.1 31.3 30.7 X2 0.0008029253 0.0008813896 0.0139181 0.000379911 0.000274224 2 R adj 0.9827 0.9324 0.8079 0.9779 0.9557 6 Journal of Insect Science, 2017, Vol. 17, No. 2

0.06 Analytis 0.06 Briere-2 ) ) -1 -1 0.05 0.05

0.04 0.04

0.03 0.03

0.02 0.02

0.01 (day rate Developmental 0.01 Developmental rate (day rate Developmental

0 0 0 5 10 15 20 25 30 35 40 45 0 5 10 15 20 25 30 35 40 45 Temperature (ºC) Temperature (ºC)

0.06 Lactin-2 0.06 SSI ) ) -1 0.05 -1 0.05

0.04 0.04

0.03 0.03

0.02 0.02 Developmental rate (day rate Developmental 0.01 (day rate Developmental 0.01

0 0 0 5 10 15 20 25 30 35 40 45 0 5 10 15 20 25 30 35 40 45 Temperature (ºC) Temperature (ºC)

Fig. 2. Fitting the nonlinear models to observed developmental rates of Glyphodes pyloalis. (•) observed data. In SSI model (᭺) indicates data points outside the range of the linear model. (h) denotes the predicted developmental rates at TL, Topt, and TH. study confirmed that at 16 C matured larvae developed to prepupae measured only at moderate temperatures (Wagner et al. 1984). The and prepupal developmental time lasted 101.68 d, suggesting that current study showed that developmental time of different stages the overwintering matured larvae in Mathur (1980) research might (egg, larva, prepupa, and pupa) of G. pyloalis decreased with be the same as prepupae. Since Mathur (1980) did not concentrate increasing temperature from 16 to 30 C, and came out from linear on the prepupal period of G. pyloalis as a distinct stage, this mode at 32 C. Assuming that developmental rate of all immature assumption seems to be presumable. No more information is cur- stages is a linear function of temperature within the 20–30 C range, rently available on overwintering of G. pyloalis, hence probability whereas a nonlinear response occurred at extreme temperature of hibernation or diapause occurrence in prepupal stage could be 32 C. Therefore, the data deviated from linearity at 32 C was proposed cautiously. excluded from linear regressions. Moreover, developmental rate of The results of the current study indicated that the egg-to-adult G. pyloalis at 16 C was omitted because very low survivorship developmental time was completed in 29.34 d at 24 C. Based on (4%) was observed at this temperature. Khosravi and Jalali Sendi (2010), total developmental time of G. According to the results of the present study, the lower develop- pyloalis were 28.77 and 29.21 d for female and male, respectively. It mental threshold for overall immature stages of G. pyloalis was esti- seems that our findings for total developmental time were consistent mated at 10.30 and 11.22 C based on traditional and Ikemoto– with those of Khosravi and Jalali Sendi (2010) at 24 C. Whereas Takai linear models, respectively. Both linear models had high val- 2 2 Oftadeh et al. (2015) reported a higher value of total developmental ues of R and R adj, indicating a high degree of confidence. It should time at 24 C in their study wherein G. pyloalis completed the devel- be noted that the higher Tmin values were estimated by traditional opment from 35.04 to 37.64 d on different mulberry varieties. (13.58 C), Ikemoto–Takai (14.93 C), Analytis (15.98 C), Briere-2 As temperature exerts noticeable influence among the climate (16.04 C), Lactin-2 (14.8 C), and SSI (16.96 C) models for prepu- factors, by directly affecting insect phenology and distribution, most pal stage compared with other stages, suggesting that the prepupal of the models that describe insect development are temperature stage showed sensitivity to lower temperatures. With regard to driven (Wagner et al. 1984). Several models have been proposed to higher Tmin values for prepupal stage of G. pyloalis compared with describe developmental rate response curves over the wide range of other (egg, larval, and pupal) stages, the prepupal stage might be temperatures, in which the linear model has the advantage of being assigned as critical stage for diapause or hibernation. Generally, low easy to calculate and is the only model enabling the estimation of temperature might enable to stop development and induce hiberna- the thermal constant (Kontodimas et al. 2004) but it can be tion at prepupal stage of G. pyloalis as Mathur (1980) observed Journal of Insect Science, 2017, Vol. 17, No. 2 7 under field conditions. However, a continued study is necessary to should be considered as the optimal temperature (Ranjbar-Aghdam determine different factors affecting diapause and overwintering of et al. 2009, Zahiri et al. 2010), ignoring the intrinsic optimum tem-

G. pyloalis, as well as physiological experiments for understanding perature (Topt) has different concepts from Tfast. In fact, the temper- the hormonal mechanisms responsible for. ature at which the population size reaches its maximum is not the

The obtained results of the present study revealed that the ther- temperature (Tfast) that can make insects develop fastest with low mal constants for overall immature stages were 429.18 and 401.88 survival and net reproductive rate. The current study showed that

DD estimated by traditional and Ikemoto–Takai linear models. the values of Topt estimated by SSI model for overall immature Considering that G. pyloalis required high thermal constant for stages of G. pyloalis was at 24.63 C, although the highest develop- completion of entire immature stages, the late incidence of G. pyloa- mental rate was estimated at 30.7 C. Based on thermodynamic con- lis during the post commercial season of mulberry could be justifi- cepts of SSI model, at Topt of 24.63 C determined for overall able. Ramegowda et al. (2012) and Borgohain et al. (2015) stated immature stages, the maximal active state enzymes involved in the that the peak of incidence and severity of G. pyloalis were distinct developmental process (Shi et al. 2011b, 2012; Padmavathi et al. during the late season and the pest damage was limited in spring 2013). The intrinsic optimum temp at which no enzyme inactivation crop of silkworm. In fact, those results could support our findings is hypothesized could represent the most important thermal parame- on high thermal constant of G. pyloalis, explaining some reasons for ter that determine the fitness of an optimum life history strategy for the pest prolonger in the late spring and summer. So far no informa- insects. Therefore, it could be proposed to evaluate the life table tion exists on temperature-dependent development of G. pyloalis parameters of G. pyloalis at different temperatures because of lack and in the current study its critical temperatures and thermal of such information. In that case, the seasonal prediction of the requirements were estimated for the first time. Hence, further phys- occurrence as well as severity of the pest would be accurately iological and ecological studies would warrant to quantify the phe- clarified. nology of G. pyloalis based on thermal requirements. Accordingly, the importance of the seasonal occurrence predic- Since the linear models is unsecure in predicting development in tion of the pest for developing management strategies has led to dif- extreme temperatures, several nonlinear models provide critical tem- ferent linear and nonlinear models that describe the developmental peratures such as lower and upper temperature thresholds, fastest rate of G. pyloalis in relation to temperature. The results of the development temperature and intrinsic optimum temperature present study could provide essential information on temperature- (Analytis 1981, Schoolfield et al. 1981, Lactin et al. 1995, Briere dependent development of G. pyloalis and its critical temperatures. et al. 1999, Ikemoto 2005, Shi et al. 2011b). To describe the devel- Using those valuable information with other ecological data such as opmental rate more realistically and over a wider temperature range, intrinsic rate of increase, survival rate and climate factors would four nonlinear models (Analytis, Briere-2, Lactin-2, and SSI) have enable researchers to predict the population dynamics of G. pyloalis been applied in the current investigation. Based on our results, the for applied IPM implementation. 2 adjusted coefficients of determination (R adj) in all mentioned non- linear models fitting to overall developmental rate were higher than 0.95, suggesting the high degree of confidence in estimated parame- Acknowledgments ters. Nonetheless, to select the models which provide satisfactory fit The authors express their gratitude to University of Guilan for financial sup- 2 to observed data, the R adj is not sufficient. It should be noticed that port. The authors are so grateful to Prof. Peijian Shi from the State Key although the Lactin-2 gave a good fit to the observed data for total Laboratory of Integrated Management of Pest and Rodents, Institute of 2 Zoology, Chinese Academy of Sciences, for useful comments on the SSI developmental times as indicated by the high values R adj, the model program. underestimated the Tmin values. Comparing the Tmin estimated by Lactin-2 using observed total developmental rate under laboratory conditions indicated that the Lactin-2 did not provide a realistic esti- Funding mate of this critical temperature. In fact, the Lactin-2 underesti- The work is a part of the M.Sc. thesis of first author which was funded by mated Tmin at 9 C, whereas failure of G. pyloalis development was University of Guilan. observed at 12 C. Furthermore, Tmin of 12.09, 12.85, and 11.13 C for egg stage estimated by the Analytis, Briere-2, and SSI models were strongly provided by experimental observations, in which, eggs References Cited of G. pyloalis could hatch at 12 C but no neonate larvae survived Analytis, S. 1981. Relationship between temperature and development times and developed to next stages. The survivorship of larvae at higher in phytopathogenic fungus and in plant pests: a mathematical model. Agric. temperatures compared with egg stage resulted in estimating the Res. (Athens). 5: 133–159. higher Tmin values for larval stage. Borgohain, A., J. Battacharjee, L. C. Dutta, B. Bhattacharya, and T. A. Our findings revealed that the Analytis, Briere-2, and SSI models Singha. 2015. Influence of climatic factors on infestation and damage of approximately provided satisfactory estimates of Tmax (36.66, mulberry plant by Glyphodes pyloalis Walker in Jorhat (Assam). J. Exp. 35.97, and 34.05 C, respectively) for total immature stages which Zool. . 18: 821–824. are consistent with those of experimental observations. Whereas the Braman, S. K., P. E. Sloderbeck, and K. V. Yeargan. 1984. Effects of tempera- ture on the development and survival of Nabis americoferus and N. rosei- Lactin-2 overestimated Tmax values for overall immature stages of G. pyloalis at 38.88 C. pennis (Hemiptera: Nabidae). Ann. Entomol. Soc. Am. 77: 592–596. Briere, J. F., P. Pracros, A. Y. Le Roux, and S. Pierre. 1999. A novel rate model Based on current study, Tfast for overall immature stages at of temperature dependent development for . Environ. Entomol. which the highest developmental rates were estimated, ranged 30.7– 28: 22–29. 31.1 C using the Analytis, Briere-2, Lactin-2, and SSI models. These Campbell, A., B. D. Frazer, N. Gilbert, A. P. Gutierrez, and M. Mackauer. four models seem to provide realistic values of Tfast because the 1974. Temperature requirements of some aphids and their parasites. J. shortest developmental time of G. pyloalis was recorded at 30 C Appl. Ecol. 11: 431–438. under laboratory conditions. Many earlier researchers documented Davidson, J. 1944. On the relationship between temperature and the rate of that the temperature, at which the developmental time is shortest, development of insects at constant temperatures. J. . Ecol. 13: 26–38. 8 Journal of Insect Science, 2017, Vol. 17, No. 2

Honek, A. 1996. Geographical variation in thermal requirements for insect de- Padmavathi, C., G. Katti, V. Sailaja, A. P. Padmakumari, V. Jhansilakshmi, velopment. Eur. J. Entomol. 93: 303–312. M. Prabhakar, and Y. G. Prasad. 2013. Temperature thresholds and thermal Ikemoto, T. 2005. Intrinsic optimum temperature for development of insects requirements for the development of the rice leaf folder, Cnaphalocrocis and mites. Environ. Entomol. 34: 1377–1387. medinalis. J. Insect Sci. 13: 1–14. Ikemoto, T. 2008. Tropical malaria does not mean hot environments. J. Med. Ramegowda, G. K., L. Illahi, V. Mittal, I. Akhter, A. Dhar, and M. A. Khan. Entomol. 45: 963–969. 2012. Influence of weather on the incidence and severity of lesser mulberry Ikemoto, T., and K. Takai. 2000. A new linearized formula for the law of total pyralid and mulberry looper in Kashmir. Indian J. Entomol. 9: 422–428. effective temperature and the evaluation of line-fitting methods with both Ranjbar-Aghdam, H., Y. Fathipour, G. Radjabi, and M. Rezapanah. 2009. variables subject to error. Environ. Entomol. 29: 671–682. Temperature dependent development and temperature thresholds of codling Jafari, S. H., Y. Fathipour, and F. Faraji. 2012. Temperature-dependent devel- (Lepidoptera: Tortricidae) in Iran. Environ. Entomol. 38: 885–895. opment of Neoseiulus barkeri (Acari: Phytoseiidae) on Tetranychus urticae Roy, M., J. Brodeur, and C. Cloutier. 2002. Relationship between temperature (Acari: Tetranychidae) at seven constant temperatures. Insect Sci. 19: and developmental rate of Stethorus punctillum (Coleoptera: Coccinellidae) 220–228. and its prey Tetranychus mcdanieli (Acarina: Tetranychidae). Environ. Karimi-Malati, A., Y. Fathipour, and A. A. Talebi. 2014. Development re- Entomol. 31: 177–187. sponse of Spodoptera exigua to eight constant temperatures: Linear and SAS Institute. 2007. JMP Statistics and Graphics Guide, Release 7. SAS nonlinear modeling. J. Asia Pac. Entomol. 17: 349–354. Institute, Cary, NC. Khosravi, R., and J. Jalali Sendi. 2010. Biology and demography of Glyphodes Schoolfield, R. M., P. J. H. Sharpe, and C. E. Magnuson. 1981. Non-linear re- pyloalis Walker (Lepidoptera: Pyralidae) on mulberry. J. Asia Pac. Entomol. gression of biological temperature-dependent rate models based on absolute reaction-rate theory. J. Theor. Biol. 88: 719–731. 13: 273–276. Sharpe, P. J. H., and D. W. DeMichele. 1977. Reaction kinetics of poikilo- Kontodimas, D. C., P. A. Eliopoulos, G. J. Stathas, and L. P. Economou. 2004. therm development. J. Theor. Biol. 64: 649–670. Comparative temperature-dependent development of Nephus includens Shi, P., F. Ge, Y. Sun, and C. Chen. 2011a. A simple model for describing the (Kirsch) and Nephus bisignatus (Boheman) (Coleoptera: Coccinellidae), effect of temperature on insect developmental rate. J. Asia Pac. Entomol. 14: preying on Planococcus citri (Risso) (Homoptera: Pseudococcidae): evalu- 15–20. ation of a linear and various non-linear models using specific criteria. Shi, P., T. Ikemoto, C. Egami, Y. Sun, and F. Ge. 2011b. A modified program Environ. Entomol. 33: 1–11. for estimating the parameters of the SSI model. Environ. Entomol. 40: Kumar, V., V. Kumar, S. Rajadurai, A. M. Babu, R. L. Katiyar, B. K. 462–469. Kariappa, V. Thiagarajan, and K. P. Jayaswal. 2002. The chronic architec- Shi, P., B. L. Li, and F. Ge. 2012. Intrinsic optimum temperature of the dia- ture and shell structure of Diaphania pulverulentalis (Hampson) mondback moth and its ecological meaning. Environ. Entomol. 41: (Lepidoptera: Pyralidae). Russ. Entomol. J. 11: 307–310. 714–722. Lactin, D. J., N. J. Holliday, D. L. Johnson, and R. Craigen. 1995. Improved Shi, P., H. S. Sandhu, and F. Ge. 2013. Could the intrinsic rate of increase rep- rate of temperature dependent development by arthropods. Environ. resent the fitness in terrestrial ectotherms? J. Therm. Biol. 38: 148–151. Entomol. 24: 68–75. Tobin, C. P., S. Nagarkatti, and M. C. Sauders. 2003. Phenology of grape Madyarov, S. R., A. S. Khamraev, D. O. Otarbaev, S. G. Kamita, and B. D. berry moth (Lepidoptera: Tortricidae) in cultivated grape at selected geo- Hammock. 2006. Comparative effects of wild and recombinant baculoviral graphic locations. Environ. Entomol. 32: 340–346. insecticides on mp Glyphodes pyloalis and mulberry silkworm Bombyx Watanabe, H., Y. Kurihara, Y. X. Wang, and T. Shimizu. 1988. Mulberry mori, pp. 230–231. In International Workshop on Silk Handcrafts Cottage pyralid, Glyphodes pyloalis: Habitual host of nonoccluded viruses patho- Industries and Silk Enterprises Development in Africa, Europe, Central Asia genic to the silkworm, Bombyx mori. J. Invertebr. Pathol. 52: 401–408. and the Near East, & Second Executive Meeting of Black, Caspian seas and Wagner, T. L., H. Wu, P. J. H. Sharpe, R. M. Schoolfield, and R. N. Coulson. Central Asia Silk Association (BACSA), 6–10 March, Bursa, Turkey. 1984. Modeling insect development rate: a literature review and application Mathur, R. N. 1980. Biology of the mulberry defoliator Glyphodes pyloalis of a biophysical model. Ann. Entomol. Soc. Am. 77: 208–225. (Lepidoptera: Pyralidae). Ind. Forest. Bull. 273: 1–6. Yazdani, E., J. Jalali Sendi, and J. Hajizadeh. 2014. Effect of Thymus vulgaris Oftadeh, M., J. Jalali Sendi, A. Zibaee, and B. Valizadeh. 2014. Effect of four L. and Origanum vulgare L. essential oils on toxicity, food consumption, varieties of mulberry on biochemistry and nutritional physiology of mul- and biochemical properties of lesser mulberry pyralid Glyphodes pyloalis berry pyralid, Glyphodes pyloalis Walker (Lepidoptera: Pyralidae). J. Walker (Lepidoptera: Pyralidae). J. Plant Prot. Res. 54: 53–61. Entomol. Acarol. Res. 46: 42–49. Zahiri, B., Y. Fathipour, M. Khanjani, S. Moharramipour, and M. Zaluki. Oftadeh, M., J. Jalali Sendi, and R. Khosravi. 2015. Life table parameters of 2010. Preimaginal development response to constant temperatures in Glyphodes pyloalis Walker (Lep.: Pyralidae) on four varieties of mulberry Hypera postica (Coleoptera: Curculionidae): picking the best model. Morus alba L. (Moraceae). J. Asia Pac. Entomol. 18: 315–320. Environ. Entomol. 39: 177–189.